Carbonate-hosted microbial communities are prolific and pervasive methane oxidizers at geologically diverse marine methane seep sites

At marine methane seeps, vast quantities of methane move through the shallow subseafloor, where it is largely consumed by microbial communities. This process plays an important role in global methane dynamics, but we have yet to identify all of the methane sinks in the deep sea. Here, we conducted a continental-scale survey of seven geologically diverse seafloor seeps and found that carbonate rocks from all sites host methane-oxidizing microbial communities with substantial methanotrophic potential. In laboratory-based mesocosm incubations, chimney-like carbonates from the newly described Point Dume seep off the coast of Southern California exhibited the highest rates of anaerobic methane oxidation measured to date. After a thorough analysis of physicochemical, electrical, and biological factors, we attribute this substantial metabolic activity largely to higher cell density, mineral composition, kinetic parameters including an elevated V_max, and the presence of specific microbial lineages. Our data also suggest that other features, such as electrical conductance, rock particle size, and microbial community alpha diversity, may influence a sample’s methanotrophic potential, but these factors did not demonstrate clear patterns with respect to methane oxidation rates. Based on the apparent pervasiveness within seep carbonates of microbial communities capable of performing anaerobic oxidation of methane, as well as the frequent occurrence of carbonates at seeps, we suggest that rock-hosted methanotrophy may be an important contributor to marine methane consumption.

The anaerobic oxidation of methane (AOM) strongly modulates the emission of a potent greenhouse gas and represents a primary production pathway that mobilizes carbon, sulfur, and nitrogen on a global scale (1–3). AOM at marine methane seeps has been estimated to consume 80% of subsurface methane (2). However, the location and magnitude of methane oxidation within seep complexes are poorly constrained because the ways in which different substrate types (e.g., sediments or rocks) influence AOM have not been adequately studied.One overlooked habitat at methane seeps is carbonate rock, which can comprise a substantial proportion of methane-perfused volume at seeps (4–9). Biomarkers and geochemical signatures suggestive of methane-oxidizing lineages—such as archaeal lipids, 16S rRNA genes, and isotopically light carbon compositions—have been detected in seep-associated carbonates (4, 10–13), but the potential role of these substrates in contemporary methane cycling has been largely neglected. Carbonate-hosted (endolithic) AOM activity has been suggested by shifts in microbial community composition (14) and explicitly demonstrated through methane oxidation rate measurements and stable isotope probing at a single location [Hydrate Ridge (15)]. Given the importance of methane in climate regulation, the presence of authigenic carbonates at seeps, and the limited but encouraging indications of rock-hosted methanotrophy to date, the extent of endolithic methane-oxidizing activity at methane seeps warranted additional study.Here, we present a continental-scale survey of sediment and endolithic microbial communities and their AOM potential at a diverse set of marine methane seeps. Sampling locations included seven sites across four geological settings: 1) the northern Gulf of Mexico, where a sedimentary basin borders a carbonate platform (16); 2) two midcontinental slope submarine canyons on the US Atlantic passive margin (17); 3) two habitats in the Gulf of California’s Guaymas Basin, a heavily sedimented, organic rich hydrothermal site (18); and 4) two seep sites—including a newly discovered field of small carbonate “chimneys” near Point Dume, CA—along the Southern California coast’s active transpressional margin (19) (Fig. 1, Dataset S1, and SI Appendix, Figs. S1–S5). We quantified methane oxidation rates at methane-saturated conditions representative of many active seeps, compared our results to previously published data within a kinetic framework, and explored the likely determinants of rate differences, including microbial abundance, community composition, and mineralogical context. Our findings revealed extremely high potential rates of AOM within select carbonate structures, validating earlier research from a more limited set of samples (15) and demonstrating that endolithic methanotrophic communities are likely ubiquitous among the substantial carbonate deposits that occur within some areas of methane seepage. We posit that seep carbonates represent a habitat with attributes that can support elevated AOM rates and that carbonate-hosted AOM may play a role in greenhouse gas sequestration and the flow of methane-derived carbon into biogeochemical cycles.Open in a separate windowFig. 1.An overview of the seven sites across four distinct geological settings that were sampled in this study. All scale bars are ∼25 cm; additional geographical and ground cover context is provided for each site in SI Appendix, Figs. S1–S5.